Skip to main content

The Acceptor Quinones of Purple Photosynthetic Bacteria — Structure and Spectroscopy

  • Chapter
The Purple Phototrophic Bacteria

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 28))

Summary

Type II reaction centers (RCs) have two acceptor quinones that act in series. The primary quinone, QA, cycles between the oxidized quinone and singly reduced semiquinone. QA is tightly bound to the protein as aprosthetic group. The secondary quinone, QB, is reduced by Q A , first to the semiquinone and then to the doubly reduced, fully protonated quinol, QH2. QB freely associates with the protein in the quinone and quinol states. The properties of the two quinones that facilitate this process are largely determined by the nature of the two quinone binding sites. Many reaction center crystal structures show these interactions, although there are significant uncertainties in the conformations of the two quinones, and in the significance of the variable location of QB in the protein. Consequently the influence of structure on quinone function is only very crudely understood. These issues are discussed with emphasis on the quinone reactions in the reaction center from the photosynthetic bacterium, Rhodobacter (Rba.) sphaeroides, which is the best characterized. The structural features of the quinones and their local protein environments are examined in the light of extensive spectroscopic studies, especially by Fourier transform infra-red spectroscopy (FTIR), electron paramagnetic resonance (EPR) and electron nuclear double resonance (ENDOR), on the quinones in their functional redox states.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Abbreviations

BChl:

bacteriochlorophyll

Bphe:

bacteriopheophytin

Blc. :

Blastochloris

DFT:

density functional theory

ENDOR:

Electron Nuclear Double Resonance

EPR:

Electron Paramagnetic Resonance

FTIR:

Fourier Transform Infrared Spectroscopy

IR:

infra-red

NMR:

Nuclear Magnetic Resonance

QA,B :

primary and secondary quinone acceptors

Rba. :

Rhodobacter

RC:

reaction center

UQ:

ubiquinone (2,3-dimethoxy -5-methyl-6-isoprenyl-1,4-benzoquinone)

References

  • Abresch EC, Paddock ML, Stowell MHB, McPhillips TM, Axelrod HL, Soltis SM, Rees DC, Okamura MY and Feher G (1998) Identification of proton transfer pathways in the X-ray crystal structure of the bacterial reaction center from Rhodobacter sphaeroides. Photosynth Res 55: 119–125

    CAS  Google Scholar 

  • Alexov E and Gunner MR (1999) Calculated protein and proton motions coupled to electron transfer: Electron transfer from QA - to QB in bacterial photosynthetic reaction centers. Biochemistry 38: 8254–8270

    Google Scholar 

  • Alexov E, Miksovska J, Baciou L, Schiffer M, Hanson DK, Sebban P and Gunner MR (2000) Modeling effects of mutations on the free energy of the first electron transfer from QA - to QB in photosynthetic reaction centers. Biochemistry 39: 5940–5952

    PubMed  CAS  Google Scholar 

  • Allen JP, Feher G, Yeates TO, Komiya H and Rees DC (1987a) Structure of the reaction center from Rhodobacter sphaeroides R-26: The cofactors. Proc Natl Acad Sci USA 84: 5730–5734

    PubMed  CAS  Google Scholar 

  • Allen JP, Feher G, Yeates TO, Komiya H and Rees DC (1987b) Structure of the reaction center from Rhodobacter sphaeroides R-26: The protein subunits. Proc Natl Acad Sci USA 84: 6162–6166

    PubMed  CAS  Google Scholar 

  • Allen JP, Feher G, Yeates TO, Komiya H and Rees DC (1988) Structure of the Reaction Center from Rhodobacter sphaeroides R-26: Protein-cofactor (quinones and Fe2+) Interactions. Proc Natl Acad Sci USA 85: 8487–8491

    PubMed  CAS  Google Scholar 

  • Allen JP, Williams JC, Graige M, Paddock ML, Labahn A, Feher G and Okamura MY (1998) Free energy dependence of the direct charge recombination from the primary and secondary quinones in reaction centers from Rhodobacter sphaeroides. Photosynth Res 55: 227–233

    CAS  Google Scholar 

  • Arnold W and Clayton RK (1960) The first step in photosynthesis: Evidence for its electronic nature. Proc Natl Acad Sci USA 46: 769–776

    PubMed  CAS  Google Scholar 

  • Arnoux B, Gaucher JF, Ducruix A and Reiss-Husson F (1995) Structure of the photochemical-reaction center of a spheroidenecontaining purple bacterium, Rhodobacter sphaeroides Y, at 3 Å resolution. Acta Crystallographica D 51: 368–379

    CAS  Google Scholar 

  • Badger RM and Bauer SH (1937) Spectroscopic studies of the hydrogen bond. II. The shift of the O-H vibrational frequency in the formation of the hydrogen bond. J Chem Phys 5: 839–851

    CAS  Google Scholar 

  • Bauscher M and Mäntele W (1992) Electrochemical and infraredspectroscopic characterization of redox reactions of p-quinones. J Phys Chem 96: 11101–11108

    CAS  Google Scholar 

  • Baxter RHG, Ponomarenko N, Srajer V, Pahl R, Moffat K and Norris JR (2004) Time-resolved crystallographic studies of light-induced structural changes in the photosynthetic reaction center. Proc Nat Acad Sci USA 101: 5982–5987

    PubMed  CAS  Google Scholar 

  • Bellamy LJ (1968) Advances in Infrared Group Frequencies. Methuen & Co. Ltd, London

    Google Scholar 

  • Bellamy LJ (1975) The Infrared Spectra of Complex Molecules. Chapman and Hall, London, New York

    Google Scholar 

  • Bellamy LJ and Pace RJ (1970) Hydrogen bonding in alcohols and phenols. III. Hydrogen bonds between alcohols and carbonyl groups. Spectrochimica Acta A 27: 705–713

    Google Scholar 

  • Beroza P, Fredkin DR, Okamura MY and Feher G (1995) Electrostatic calculations of amino acid titration electron transfer, QA -QB → QAQB -, in the reaction center. Biophys J 68: 2233–2250

    PubMed  CAS  Google Scholar 

  • Blankenship RE and Parson WW (1979) The involvement of iron and ubiquinone in electron transfer reactions mediated by reaction centers from photosynthetic bacteria. Biochim Biophys Acta 545: 429–444

    PubMed  CAS  Google Scholar 

  • Bloom H, Briggs LH and Cleverley B (1959) Physical properties of anthraquinone and its derivatives. Part I. Infrared spectra. J Chem Soc 1959: 178–185

    Google Scholar 

  • Boesch SE and Wheeler RA (1997) Structures and properties of ubiquinone-1 and its radical anion predicted from a hybrid Hartree-Fock/density functional method. J Phys Chem A 101: 5799–5804

    CAS  Google Scholar 

  • Bosch MK, Gast P, Hoff AJ, Spoyalov AP and Tsvetkov YD (1995) The primary acceptor quinone QA in reaction centers of Rhodobacter sphaeroides R26 is hydrogen bonded to the Nδ (1)-H of His M219. An electron spin echo study of QA -•. Chem Phys Lett 239: 306–312

    CAS  Google Scholar 

  • Boullais C, Nabedryk E, Burie J-R, Nonella M, Mioskowski C and Breton J (1998) Site-specific isotope labeling demonstrates a large mesomeric resonance effect of the methoxy groups on the carbonyl frequency in ubiquinones. Photosynth Res 55: 247–252

    CAS  Google Scholar 

  • Breen, DL (1975) Coenzyme Q: A molecular orbital study. J Theor Biol 53: 101–113

    PubMed  CAS  Google Scholar 

  • Breton J (2004) Absence of large-scale displacement of quinone QB in bacterial photosynthetic reaction centers. Biochemistry 43: 3318–3326

    PubMed  CAS  Google Scholar 

  • Breton J and Nabedryk E (1995) Protein and bacteriopheophytin response to QA reduction in photosynthetic bacterial reaction centers from Rb. sphaeroides and Rp. viridis investigated by 1H/2H exchange and light-induced FTIR difference spectroscopy. In: Mathis P (ed) Photosynthesis: From Light to Biosphere, Vol I, pp 395–400. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Breton J and Nabedryk E (1996) Protein-quinone interactions in the bacterial photosynthetic reaction center: Light-induced FTIR difference spectroscopy of the quinone vibrations. Biochim Biophys Acta 1275: 84–90

    Google Scholar 

  • Breton J, Boullais C, Burie J, Nabedryk E and Mioskowski C (1994a) Binding sites of quinones in photosynthetic bacterial reaction centers investigated by light-induced FTIR difference spectroscopy: Assignment of the interactions of each carbonyl of QA in Rhodobacter sphaeroides using site-specific 13C-labeled ubiquinone. Biochemistry 33: 14378–14386

    PubMed  CAS  Google Scholar 

  • Breton J, Burie J, Boullais C, Berger G and Nabedryk E (1994b) Binding sites of quinones in photosynthetic bacterial reaction centers investigated by light-induced FTIR difference spectroscopy: Binding of chainless symmetrical quinones to the QA site of Rhodobacter sphaeroides. Biochemistry 33: 12405–12415

    PubMed  CAS  Google Scholar 

  • Breton J, Burie J-R, Berthomieu C, Berger G and Nabedryk E (1994c) The binding sites of quinones in photosynthetic bacterial reaction centers investigated by light-induced FTIR difference spectroscopy: Assignment of the QA vibrations in Rhodobacter sphaeroides using 18O- or 13C-labeled ubiquinone and vitamin K1. Biochemistry 33: 4953–4965

    PubMed  CAS  Google Scholar 

  • Breton J, Boullais C, Berger G, Mioskowski C and Nabedryk E (1995) Binding sites of quinones in photosynthetic bacterial reaction centers investigated by light induced FTIR difference spectroscopy: symmetry of the carbonyl interactions and close equivalence of the QB vibrations in Rhodobacter sphaeroides and Rhodopseudomonas viridis probed by isotopic labeling. Biochemistry 34: 11606–11616

    PubMed  CAS  Google Scholar 

  • Breton J, Boullais C, Mioskowski C, Sebban P, Baciou L and Nabedryk E (2002) Vibrational spectroscopy favors a unique QB binding site at the proximal position in wild-type reaction centers and in the Pro-L209→Tyr mutant from Rhodobacter sphaeroides. Biochemistry 41: 12921–12927

    PubMed  CAS  Google Scholar 

  • Breton J, Wakeham MC, Fyfe PK, Jones MR and Nabedryk E (2004) Characterization of the bonding interactions of QB upon photoreduction via A-branch or B-branch electron transfer in mutant reaction centers from Rhodobacter sphaeroides. Biochim Biophys Acta 1656: 127–138

    PubMed  CAS  Google Scholar 

  • Breton J, Lavergne J, Wakeham MC, Nabedryk E and Jones MR (2007) The unusually strong hydrogen bond between the carbonyl of QA and His M219 in the Rhodobacter sphaeroides reaction center is not essential for efficient electron transfer from QA - to QB. Biochemistry 46: 6468–6476

    PubMed  CAS  Google Scholar 

  • Bruce BD, Fuller RC and Blankenship RE (1982) Primary photosynthesis in the facultative aerobic green photosynthetic bacterium Chloroflexus aurantiacus. Proc Natl Acad Sci USA 79: 6532–6536

    PubMed  CAS  Google Scholar 

  • Brudler R, de Groot HJM, van Liemt WBS, Steggerda WF, Esmeijer R, Gast P, Hoff AJ, Lugtenburg J and Gerwert K (1994) Asymmetric binding of the 1- and 4-C=O groups of QA in Rhodobacter sphaeroides R26 reaction centers monitored by Fourier transform infra-red spectroscopy using site-specific isotopically labelled ubiquinone-10. EMBO J 13: 5523–5530

    PubMed  CAS  Google Scholar 

  • Brudler R, de Groot HJM, van Liemt WBS, Hoff AJ, Lugtenburg JL and Gerwert K (1995) FTIR spectroscopy shows weak symmetric hydrogen bonding of the QB carbonyl groups in Rhodobacter sphaeroides R26 reaction centres. FEBS Lett 370: 2–14

    Google Scholar 

  • Burie J-R, Boussac A, Boullas C, Berger G, Mattioli T, Mioskowski C, Nabedryk E and Breton J (1995) FTIR spectroscopy of UV-generated quinone radicals: Evidence for an intramolecular hydrogen atom transfer in ubiquinone, naphthoquinone, and plastoquinone. J Phys Chem B 99: 4059–4070

    CAS  Google Scholar 

  • Burie J-R, Boullais C, Nonella M, Mioskowski C, Nabedryk E and Breton J (1997) Importance of the conformation of methoxy groups on the vibrational and electrochemical properties of ubiquinones. J Phys Chem B 101: 6607–6617

    CAS  Google Scholar 

  • Burley SK and Petsko GA (1985) Aromatic-aromatic interaction: A mechanism of protein structure stabilization. Science 229: 23–28

    PubMed  CAS  Google Scholar 

  • Butler WF, Johnston DC, Shore HB, Fredkin DR, Okamura MY and Feher G (1980) The electronic structure of Fe2+ in reaction centers from Rhodopseudomonas sphaeroides I. Static magnetization measurements. Biophys J 32: 967–992

    PubMed  CAS  Google Scholar 

  • Butler WF, Calvo R, Fredkin DR, Isaacson RA, Okamura MY and Feher G (1984) The electronic structure of Fe2+ in reaction centers from Rhodopseudomonas sphaeroides III. EPR measurements of the reduced acceptor complex. Biophys J 45: 947–973

    PubMed  CAS  Google Scholar 

  • Chang C-H, El-Kabbani O, Tiede D, Norris J and Schiffer M (1991) Structure of the membrane-bound protein photosynthetic reaction center from Rhodobacter sphaeroides. Biochemistry 30: 5352–5360

    PubMed  CAS  Google Scholar 

  • Chirino AJ, Lous EJ, Huber M, Allen JP, Schenck CC, Paddock ML, Feher G and Rees DC (1994) Crystallographic analyses of site-directedmutants of the photosynthetic reaction center from Rhodobacter sphaeroides. Biochemistry 33: 4584–4593

    PubMed  CAS  Google Scholar 

  • Coleman WJ, Bylina EJ and Youvan DC (1990a) Reconstitution of photochemical activity in Rhodobacter capsulatus reaction centers containing mutations at trytophan M-250 in the primary quinone binding site. In: Baltscheffsky M (ed) Current Research in Photosynthesis, Vol 1, pp 149–152. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Coleman WJ, Youvan DC, Aumeier W, Eberl U, Volk M, Lang E, Siegl J, Heckmann R, Lersch W, Ogrodnik A and Michel-Beyerle ME (1990b) How conclusive is mutagenic replacement of Trp M250 in photosynthetic reaction centers? In: Baltscheffsky M (ed) Current Research in Photosynthesis, Vol 1, pp 153–156. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • De Groot HJM (1995) Asymmetric primary quinone hydrogen bonding in Rhodobacter sphaeroides reaction centers. In: Mathis P (ed) Photosynthesis: From Light to Biosphere, I, pp 401–406. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Deisenhofer J and Michel H (1989a) The photosynthetic reaction center from the purple bacterium Rhodopseudomonas viridis. Science 245: 1463–1473

    PubMed  CAS  Google Scholar 

  • Deisenhofer J and Michel H (1989b) The photosynthetic reaction centre from the purple bacterium Rhodopseudomonas viridis. EMBO J 8: 2149–2170

    PubMed  CAS  Google Scholar 

  • Deisenhofer J and Michel H (1991) High-resolution structures of photosynthetic reaction centers. Annu Rev Biophys Chem 20: 247–266

    CAS  Google Scholar 

  • Deisenhofer J, Epp O, Miki R, Huber R and Michel H (1985) Structure of the protein subunits in the photosynthetic reaction center of Rhodopseudomonas viridis at 3 Å resolution. Nature 318: 618–624

    Google Scholar 

  • Deng H and Callender R (1999) Raman spectroscopic studies of the structure, energetics, and bond distortions of substrates bound to enzymes. Methods Enzymol 308: 176–201

    PubMed  CAS  Google Scholar 

  • DeVault D (1980) Quantum-mechanical tunneling in biological systems. Q Rev Biophys 13: 387–564

    PubMed  CAS  Google Scholar 

  • El-Kabbani O, Chang C-H, Tiede D, Norris J and Schiffer M (1991) Comparison of reaction centers from Rhodobacter sphaeroides and Rhodopseudomonas viridis: Overall architecture and protein-pigment interactions. Biochemistry 30: 5361–5369

    PubMed  CAS  Google Scholar 

  • Ermler U, Fritzsch G, Buchanan SK and Michel H (1994) Structure of the photosynthetic reaction center from Rhodobacter sphaeroides at 2.65 Å resolution: Cofactors and protein-cofactor interactions. Structure 2: 925–936

    PubMed  CAS  Google Scholar 

  • Feher G, Okamura MY and McElroy JD (1972) Identification of an electron acceptor in reaction centers of Rhodopseudomonas spheroides by EPR spectroscopy. Biochim Biophys Acta 267: 222–226

    PubMed  CAS  Google Scholar 

  • Feher G, Isaacson RA, Okamura MY and Lubitz W (1985) ENDOR of semiquinones in reaction centers from Rhodopseudomonas sphaeroides. In: Michel-Beyerle ME (ed) Antennas and Reaction Centers of Photosynthetic Bacteria—Structure, Interactions and Dynamics, pp 174–189. Springer-Verlag, Berlin

    Google Scholar 

  • Feher G, Isaacson RA, Okamura MY and Lubitz W (1988). ENDOR of exchangeable protons of the reduced intermediate acceptor in reaction centers from Rhodobacter sphaeroides R-26. In: Breton J and Verméglio A (eds) The Photosynthetic Bacterial Reaction Center, Cadarache, France, Plenum Press

    Google Scholar 

  • Ferreira KN, Iverson TM, Maghlaoui K, Barber J and Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303: 1831–1838

    PubMed  CAS  Google Scholar 

  • Fisher N and Rich PR (2000) A motif for quinone binding sites in respiratory and photosynthetic systems. J Mol Biol 296: 1153–1162

    PubMed  CAS  Google Scholar 

  • Flett MSC (1948) The application of infra-red spectroscopy to structural problems in the anthraquinone field. J Chem Soc 1948: 1441–1448

    Google Scholar 

  • Flores M, Isaacson RA, Calvo R, Feher G and Lubitz W (2003) Probing hydrogen bonding to quinone anion radicals by 1H and 2H ENDOR spectroscopy at 35 GHz. Chem Phys 294: 401–413

    CAS  Google Scholar 

  • Flores M, Isaacson R, Abresch E, Calvo R, Lubitz W and Feher G (2006) Protein-cofactor interactions in bacterial reaction centers from Rhodobacter sphaeroides R-26: I. Identification of the ENDOR lines associated with the hydrogen bonds to the primary quinone QA -. Biophys J 90: 3356–3362

    PubMed  CAS  Google Scholar 

  • Flores M, Isaacson R, Abresch E, Calvo R, Lubitz W and Feher G (2007) Protein-cofactor interactions in bacterial reaction centers from Rhodobacter sphaeroides R-26: II. Geometry of the hydrogen bonds to the primary quinone QA •- by 1H and 2H ENDOR spectroscopy. Biophys J 92: 671–682

    PubMed  CAS  Google Scholar 

  • Franzen S, Goldstein RF and Boxer SG (1990) Electric field modulation of electron transfer reaction rates in isotropic systems: Long distance charge recombination in photosynthetic reaction centers. J Phys Chem 94: 5135–5149

    CAS  Google Scholar 

  • Fritscher J, Prisner TF and MacMillan F (2006) Theoretical investigation of QA -ligand interactions in bacterial reaction centers of Rhodobacter sphaeroides. Appl Mag Res 30: 251–268

    Article  CAS  Google Scholar 

  • Fritzsch G, Koepke J, Diem R, Kuglstatter A and Baciou L (2002) Charge separation induces conformational changes in the photosynthetic reaction centre of purple bacteria. Acta Cryst D 58: 1660–1663

    Google Scholar 

  • Gast P, Michalski,TJ, Hunt JE and Norris JR (1985) Determination of the amount and the type of quinones present in single crystals from reaction center protein from the photosynthetic bacterium Rhodopseudomonas viridis. FEBS Lett 179: 325–328

    CAS  Google Scholar 

  • Giangiacomo KM and Dutton PL (1989) In photosynthetic reaction centers, the free energy difference for electron transfer between quinones bound at the primary and secondary quinonebinding sites governs the observed secondary site specificity. Proc Natl Acad Sci USA 86: 2658–2662

    PubMed  CAS  Google Scholar 

  • Gordy W (1940) Spectroscopic evidence for hydrogen bonds: Effects of chelation on the carbonyl frequency. J Chem Phys 8: 516–519

    CAS  Google Scholar 

  • Grafton AK and Wheeler RA (1999) Amino acid protonation states determine binding sites of the secondary ubiquinone and its anion in the Rhodobacter sphaeroides photosynthetic reaction center. J Phys Chem B 103: 5380–5387

    CAS  Google Scholar 

  • Graige MS, Paddock ML, Bruce JM, Feher G and Okamura MY (1996) Mechanism of proton-coupled electron transfer for quinone (QB) reduction in reaction centers of Rb. sphaeroides. J Am Chem Soc 118: 9005–9016

    CAS  Google Scholar 

  • Graige MS, Feher G and Okamura MY (1998) Conformational gating of the electron transfer reaction QA -•QB → QAQB -• in bacterial reaction centers of Rhodobacter sphaeroides determined by a driving force assay. Proc Natl Acad Sci USA 95: 11679–11684

    PubMed  CAS  Google Scholar 

  • Graige MS, Paddock ML, Feher G and Okamura MY (1999) Observation of the protonated semiquinone intermediate in isolated reaction centers from Rhodobacter sphaeroides: Implications for the mechanism of electron and proton transfer in proteins. Biochemistry 38: 11465–11473

    PubMed  CAS  Google Scholar 

  • Gunner MR and Dutton PL (1989) Temperature and -ΔG dependence of the electron transfer from BPh•- to QA in reaction center protein from Rhodobacter sphaeroides with different quinones as QA. J Am Chem Soc 111: 3400–3412.

    CAS  Google Scholar 

  • Gunner MR, Braun BS, Bruce JM and Dutton PL (1985) The characterization of the QA binding site of the reaction center of Rhodopseudomonas sphaeroides. In: Michel-Beyerle ME (ed) Antennas and Reaction Centers of Photosynthetic Bacteria: Structure, Interactions and Dynamics, pp 298–304. Springer-Verlag, Berlin

    Google Scholar 

  • Gunner MR, Robertson DE and Dutton PL (1986) Kinetic studies on the reaction center protein from Rhodopseudomonas sphaeroides: The temperature and free energy dependence of electron transfer between various quinones in the QA site and the oxidized bacteriochlorophyll dimer. J Phys Chem 90: 3783–3795

    CAS  Google Scholar 

  • Gunner MR, Saleh MA, Cross E, ud-Doula A and Wise M (2000) Backbone dipoles generate positive potential in all proteins: Origins and implications of the effect. Biophys J 78: 1126–1144

    PubMed  CAS  Google Scholar 

  • Heathcote P, Fyfe PK and Jones MR (2002) Reaction centres: The structure and evolution of biological solar power. Trends Biochem Sci 27: 79–87

    PubMed  CAS  Google Scholar 

  • Heinen U, Utschig LM, Poluektov OG, Link G, Ohmes E and Kothe G (2007) Structure of the charge separated state P865+QA - in the phootosynthetic reaction centers of Rhodobacter sphaeroides by quantum beat oscillations and high-field electron paramagnetic resonance: Evidence for light-induced QA - reorientation. J Am Chem Soc 129: 15935–15946

    PubMed  CAS  Google Scholar 

  • Hucke O, Schmid R and Labahn A (2002) Exploring the primary electron acceptor (QA)-site of the bacterial reaction center from Rhodobacter sphaeroides. Binding mode of vitamin K derivatives. Eur J Biochem 269: 1096–1108

    PubMed  CAS  Google Scholar 

  • Isaacson RA, Lendzian F, Abresch C, Lubitz W and Feher G (1995) Electronic structure of QA - in reaction centers from Rhodobacter sphaeroides. I. Electron paramagnetic resonance in single crystals. Biophys J 69: 311–322

    PubMed  CAS  Google Scholar 

  • Isaacson RA, Abresch EC, Lendzian F, Boullais C, Paddock ML, Mioskowski C, Lubitz W and Feher G (1996). Asymmetry of the binding sites of QA - and QB - in reaction centers of Rb. sphaeroides probed by Q-Band EPR with 13C-labeled quinones. In: Michel-Beyerle ME (ed) The Reaction Center of Photosynthetic Bacteria: Structure and Dynamics, pp 353–368. Springer-Verlag, Berlin

    Google Scholar 

  • Ishikita H, Morra G and Knapp E-W (2003) Redox potential of quinones in photosynthetic reaction centers from Rhodobacter sphaeroides: Dependence on protonation of Glu-L212 and Asp-L213. Biochemistry 42: 3882–3892

    PubMed  CAS  Google Scholar 

  • Kacprzak S and Kaupp M (2004) Electronic g-tensors of semiquinones in photosynthetic reaction centers. A density functional study. J Phys Chem B 108: 2464–2469

    CAS  Google Scholar 

  • Katona G, Snijder A, Gourdon P, Andréasson U, Hansson Ö, Andréasson L-E and Neutze R (2005) Conformational regulation of charge recombination in a photosynthetic bacterial reaction center. Nature Struct Mol Biol 12: 630–631

    CAS  Google Scholar 

  • Kaupp M (2002) The function of Photosystem I. Quantum chemical insight into the role of tryptophan-quinone interactions. Biochemistry 41: 2895–2900

    PubMed  CAS  Google Scholar 

  • Kim J, Mao J and Gunner MR (2005) Are acidic and basic groups in buried proteins predicted to be ionized? J Mol Biol 348: 1283–1298

    PubMed  CAS  Google Scholar 

  • Kirmaier C and Holten D (1990) Evidence that a distribution of bacterial reaction centers underlies the temperature and detection-wavelength dependence of the rates of the primary electrontransfer reactions. Proc Natl Acad Sci USA 87: 3552–3556

    PubMed  CAS  Google Scholar 

  • Kleinfeld D, Okamura MY and Feher G (1984a) Electron-transfer kinetics in photosynthetic reaction centers cooled to cryogenic temperatures in the charge separated state: Evidence for lightinduced structural changes. Biochemistry 23: 5780–5786

    PubMed  CAS  Google Scholar 

  • Kleinfeld D, Okamura MY and Feher G (1984b) Electron transfer in reaction centers of Rhodopseudomonas sphaeroides: I. Determination of the charge recombination pathway of D+QAQB - and free energy and kinetic relations between QA -QB and QAQB -. Biochim Biophys Acta 766: 126–140

    PubMed  CAS  Google Scholar 

  • Koepke J, Krammer EM, Klingen AR, Sebban P, Ullmann GM and Fritzsch G (2007) pH modulates the quinone position in the photosynthetic reaction center from Rhodobacter sphaeroides in the neutral and charge separated states. J Mol Biol 371: 396–409

    PubMed  CAS  Google Scholar 

  • Krivanek R, Kern J, Zouni A, Dau H and Haumann M (2007) Spare quinones in the QB cavity of crystallized Photosystem II from Thermosynechocoecus elongatus. Biochim Biophys Acta 1767: 520–527

    PubMed  CAS  Google Scholar 

  • Kruk J, Strzalka K and Leblanc RM (1993) Fourier transform infrared studies on charge-transfer interactions of plastoquinones and α-tocopherol quinone with their hydroquinone forms and monogalactosyldiacylglycerol. Biophysical Chemistry 45: 235–244

    CAS  Google Scholar 

  • Kuglstatter A, Ermler U, Michel H, Baciou L and Fritzsch G (2001) X-ray structure analysis of photosynthetic reaction center variants from Rhodobacter sphaeroides: Structural changes induced by point mutations at position L209 modulate electron and proton transfer. Biochemistry 40: 4253–4260

    PubMed  CAS  Google Scholar 

  • Labahn A, Bruce JM, Okamura MY and Feher G (1995) Direct charge recombination from D+QAQB - to DQAQB in bacterial reaction centers from Rhodobacter sphaeroides containing low potential quinone in the QA site. Chem Phys 197: 355–366

    CAS  Google Scholar 

  • Laible PD, Kirmaier C, Udawatte CS, Hofman SJ, Holten D and Hanson DK (2003) Quinone reduction via secondary B-branch electron transfer in mutant bacterial reaction centers. Biochemistry 42: 1718–1730

    PubMed  CAS  Google Scholar 

  • Lancaster CRD (1998) Ubiquinone reduction and protonation in photosynthetic reaction centres from Rhodopseudomonas viridis — X-ray structures and their functional implications. Biochim Biophys Acta 1365: 143–150

    CAS  Google Scholar 

  • Lancaster CRD and Michel H (1996a) New Insights into the X-ray structure of the reaction center of Rhodopseudomonas viridis. In: Michel-Beyerle ME (ed) The Reaction Center of Photosynthetic Bacteria: Structure and Dynamics, pp 23–35. Springer-Verlag, Berlin

    Google Scholar 

  • Lancaster CRD and Michel H (1996b) Three-dimensional structures of photosynthetic reaction centers. Photosynth Res 48: 65–74

    CAS  Google Scholar 

  • Lancaster CRD and Michel H (1997) The coupling of light-induced electron transfer and proton uptake as derived from crystal structures of reaction centres from Rhodopseudomonas viridis modified at the binding site of the secondary quinone, QB. Structure 5: 1339–1359

    PubMed  CAS  Google Scholar 

  • Lancaster CRD, Michel H, Honig B and Gunner MR (1996) Calculated coupling of electron and proton transfer in the photosynthetic reaction center of Rhodopseudomonas viridis. Biophys J 70: 2469–2492

    PubMed  CAS  Google Scholar 

  • Lavergne J, Matthews C and Ginet N (1999) Electron and proton transfer on the acceptor side of the reaction center in chromatophores of Rhodobacter capsulatus: Evidence for direct protonation of the semiquinone state of QB. Biochemistry 38: 4542–4552

    PubMed  CAS  Google Scholar 

  • Leigh JS and Dutton PL (1972) The primary electron acceptor in photosynthesis. Biochem Biophys Res Comm 46: 414–421

    PubMed  CAS  Google Scholar 

  • Lendzian F, Rautter J, Käß H, Gardiner A and Lubitz W (1996) ENDOR and pulsed EPR studies of photosynthetic reaction centers: Protein-cofactor interactions. Ber Bunsenges Phys Chem 100: 2036–2040

    CAS  Google Scholar 

  • Li J, Gilroy D, Tiede DM and Gunner MR (1998) Kinetic phases in the electron transfer from P+QA -QB to P+QAQB - and the associated processes in Rhodobacter sphaeroides R-26 reaction centers. Biochemistry 37: 2818–2829

    PubMed  CAS  Google Scholar 

  • Li J, Takahashi E and Gunner MR (2000) -ΔG AB o and pH dependence of the electron transfer from P+QA -QB to P+QAQB - in Rhodobacter sphaeroides reaction centers. Biochemistry 39: 7445–7454

    PubMed  CAS  Google Scholar 

  • Lin X, Murchison HA, Nagarajan V, Parson WW, Allen JP and Williams JC (1994) Specific alterations of the oxidation potential of the electron donor in reaction centers from Rhodobacter sphaeroides. Proc Natl Acad Sci USA 91: 10265–10269

    PubMed  CAS  Google Scholar 

  • Loll B, Kern J, Saenger W, Zouni A and Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438: 1040–1044

    PubMed  CAS  Google Scholar 

  • Lubitz W and Feher G (1999) The primary and secondary acceptors in bacterial photosynthesis III. Characterization of the quinone radicals QA -• and QB -• by EPR and ENDOR. Appl Magn Res 17: 1–48

    CAS  Google Scholar 

  • Lubitz W, Abresch EC, Debus RJ, Isaacson RA, Okamura MY and Feher G (1985) Electron nuclear double resonance of semiquinones in reaction centers of Rhodopseudomonas sphaeroides. Biochim Biophys Acta 808: 464–469

    PubMed  CAS  Google Scholar 

  • Mancino LJ, Dean DP and Blankenship RE (1984) Kinetics and thermodynamics of the P870+QA - → P870+QB - reaction in isolated reaction centers from the photosynthetic bacterium Rhodopseudomonas sphaeroides. Biochim Biophys Acta 764: 46–54

    CAS  Google Scholar 

  • Marcus RA (1964) Chemical and electrochemical electron-transfer theory. Ann Rev Phys Chem 15: 155–196

    CAS  Google Scholar 

  • Marcus RA and Sutin N (1985) Electron transfers in chemistry and biology. Biochim Biophys Acta 811: 265–322

    CAS  Google Scholar 

  • McComb JC, Stein RR and Wraight CA (1990) Investigations on the influence of headgroup substitution and isoprene side-chain length in the function of primary and secondary quinones of bacterial reaction centers. Biochim Biophys Acta 1015: 156–171

    PubMed  CAS  Google Scholar 

  • McMahon BH, Müller JD, Wraight CA and Nienhaus GU (1998) Electron transfer and protein dynamics in the photosynthetic reaction center. Biophys J 74: 2567–2587

    PubMed  CAS  Google Scholar 

  • Meyerson ML (1985) A quantitative model for carbonyl infrared frequencies of substituted quinones. Spectrochim Acta A 41: 1263–1267

    Google Scholar 

  • Mezzetti A, Leibl W, Breton J and Nabedryk E (2003) Photoreduction of the quinone pool in the bacterial photosynthetic membrane: Identification of infrared marker bands for quinol formation. FEBS Lett 537: 161–165

    PubMed  CAS  Google Scholar 

  • Moser CC, Keske JM, Warncke K, Farid RS and Dutton PL (1992) Nature of biological electron transfer. Nature 355: 796–802

    PubMed  CAS  Google Scholar 

  • Moser CC, Page CC, Farid R and Dutton PL (1995) Biological electron transfer. J Bioenerg Biomemb 27: 263–274

    CAS  Google Scholar 

  • Moser CC, Page CC, Cogdell RJ, Barber J, Wraight CA and Dutton PI, (2003) Length, time and energy scales of photosystems. Advances Protein Chem 63: 71–109

    PubMed  CAS  Google Scholar 

  • Nabedryk E and Breton J (2008) Coupling of electron transfer to proton uptake at the QB site of the bacterial reaction center: A perspective from FTIR difference spectroscopy. Biochim Biophys Acta, in press

    Google Scholar 

  • Nogi T, Fathir I, Kobayashi M, Nozawa T and Miki K (2000) Crystal structures of photosynthetic reaction center and highpotential iron-sulfur protein from Thermochromatium tepidum: Thermostability and electron transfer. Proc Nat Acad Sci USA 97: 13561–13566

    PubMed  CAS  Google Scholar 

  • Nonella M (1997) Structure and vibrational spectra of p-benzo-quinone in different oxidation and protonation states: A density functional study. J Phys Chem B 101: 1235–1246

    CAS  Google Scholar 

  • Nonella M (1998) A quantum chemical investigation of structures, vibrational spectra and electron affinities of the radicals of quinone model compounds. Photosynth Res 55: 253–259

    CAS  Google Scholar 

  • Nonella M and Brändli C (1996) Density functional investigation of methoxy-substituted p-benzoquinones: Conformational analysis and harmonic force fields of 2-methoxy- and 2,3-dimethoxy-1,4-benzoquinone. J Phys Chem 100: 14549–14559

    CAS  Google Scholar 

  • Nonella M, Mathias G, Eichinger M and Tavan P (2003) Structures and vibrational frequencies of the quinones of Rb. sphaeroides derived by a combined density functional/molecular mechanics approach. J Phys Chem B 107: 316–322

    CAS  Google Scholar 

  • Okamura MY and Feher G (1986) Isotope effect on electron transfer in reaction centers from Rhodopseudomonas sphaeroides. Proc Natl Acad Sci USA 83: 8152–8156

    PubMed  CAS  Google Scholar 

  • Okamura MY and Feher G (1992) Proton transfer in reaction centers from photosynthetic bacteria. Annu Rev Biochem 61: 861–896

    PubMed  CAS  Google Scholar 

  • Okamura MY and Feher G (1995) Proton-coupled electron transfer reactions of QB in reaction centers from photosynthetic bacteria. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria (Advances in Photosynthesis and Respiration, Vol 2, pp 577–593. Kluwer Academic Publishers

    Google Scholar 

  • Okamura MY, Isaacson RA and Feher G (1975) The primary acceptor in bacterial photosynthesis: Obligatory role of ubiquinone in photoactive reaction centers of Rhodopseudomonas sphaeroides. Proc Natl Acad Sci USA 72: 3492–3496

    Google Scholar 

  • Okamura MY, Paddock ML, Graige MS and Feher G (2000) Proton and electron transfer in bacterial reaction centers. Biochim Biophys Acta 1458: 148–163

    PubMed  CAS  Google Scholar 

  • O’Malley PJ (1997a) A density functional study of the effect of reduction on the geometry and electron affinity of hydrogen bonded 1,4-benzoquinone. Implications for quinone reduction and protonation in photosynthetic reaction centers. Chem Phys Lett 274: 251–254

    CAS  Google Scholar 

  • O’Malley PJ (1997b) Hybrid density functional study of the p-benzosemiquinone anion radical: The influence of hydrogen bonding on geometry and hyperfine couplings. J Phys Chem A 101: 6334–6338

    CAS  Google Scholar 

  • O’Malley PJ (2001) Electronic structure studies of quinones and semiquinones: Accurate calculation of spin densities and electron paramagnetic resonance parameters. Antioxid Redox Signal 3: 825–838

    PubMed  CAS  Google Scholar 

  • O’Malley PJ (2003) The origin of the spin density asymmetry at the QA binding site of type II photosynthetic reaction centres. Chem Phys Lett 379: 277–281

    CAS  Google Scholar 

  • Paddock ML, Abresch EC, Isaacson RA, Lubitz W, Okamura MY and Feher G (1999) Identification of hydrogen bonds to QA in RCs of Rb. sphaeroides by ENDOR spectroscopy. Biophys J 76: A141

    Google Scholar 

  • Paddock ML, Feher G and Okamura MY (2003) Proton transfer pathways and mechanism in bacterial reaction centers. FEBS Lett 555: 45–50

    PubMed  CAS  Google Scholar 

  • Paddock ML, Flores M, Isaacson R, Chang C, Selvaduray P, Feher G and Okamura MY (2005) Hydrogen bond reorientation upon QB reduction revealed by ENDOR spectroscopy in reaction centers from Rhodobacter sphaeroides. Biophys J 88: 204a

    Google Scholar 

  • Paddock ML, Flores M, Isaacson R, Chang C, Abresch EC, Selvaduray P and Okamura MY (2006) Trapped conformational states of semiquinone (D+•QB -•) formed by B-branch electron transfer at low temperature in Rhodobacter sphaeroides reaction centers. Biochemistry 45: 14032–14042

    PubMed  CAS  Google Scholar 

  • Paddock ML, Flores M, Isaacson R, Chang C, Abresch EC and Okamura MY (2007) ENDOR spectroscopy reveals light induced movement of the H-bond from Ser-L223 upon forming the semiquinone (QB -•) in reaction centers from Rhodobacter sphaeroides. Biochemistry 46: 8234–8243

    PubMed  CAS  Google Scholar 

  • Parson WW (1978) Quinones as secondary electron acceptors. In: Clayton RK and Sistrom WR (eds) The Photosynthetic Bacteria, pp 455–469. Plenum, New York

    Google Scholar 

  • Plato M, Michel-Beyerle ME, Bixon M and Jortner J (1989) On the role of tryptophan as a superexchange mediator for quinone reduction in photosynthetic reaction centers. FEBS Lett 249: 70–74

    CAS  Google Scholar 

  • Pokkuluri PR, Laible PD, Deng Y-L, Wong TN, Hanson DK and Schiffer M (2002) The structure of amutantphotosynthetic reaction center shows unexpected changes in main chain orientations and quinone position. Biochemistry 41: 5998–6007

    PubMed  CAS  Google Scholar 

  • Pokkuluri PR, Laible PD, Crawford AE, Mayfield JF, Yousef MA, Ginell SL, Hanson DK and Schiffer M (2004) Temperature and cryoprotectant influence secondary quinone binding position in bacterial reaction centers. FEBS Lett 570: 171–174

    PubMed  CAS  Google Scholar 

  • Prince RC, Dutton PL and Bruce JM (1983) Electrochemistry of ubiquinones, menaquinones and plastoquinones in aprotic solvents. FEBS Lett 160: 273–276

    CAS  Google Scholar 

  • Prince RC, Halbert TR and Upton TH (1988) Structural influences on the electrochemistry of ubiquinone. In: Kim CH, Tedeschi H, Diwan JJ and Salerno JC (eds) Advances in Membrane Biochemistry and Bioenergetics, pp 469–478. Plenum Press, New York

    Google Scholar 

  • Rabenstein B, Ullmann GM and Knapp E-W (2000) Electron transfer between the quinones in the photosynthetic reaction center and its coupling to conformational changes. Biochemistry 39: 10487–10496

    PubMed  CAS  Google Scholar 

  • Rao CNR, Dwivedi PC, Ratajczak H and Orville-Thomas WJ (1975) Relation between O-H stretching frequency and hydrogen bond energy: Re-examination of the Badger-Bauer rule. J Chem Soc Faraday Trans II 71: 955–966

    CAS  Google Scholar 

  • Rasmussen RS, Tunnicliff DD and Brattain RR (1949) Infrared and ultraviolet spectroscopic studies on ketones. J Am Chem Soc 71: 1068–1072

    CAS  Google Scholar 

  • Remy A, Boers RB, Egorova-Zachernyuk T, Gast P, Lugtenberg J and Gerwert K (2003) Does different orientation of the methoxy groups of ubiquinone-10 in the reaction center of Rhodobacter sphaeroides cause different binding at QA and QB? Eur J Biochem 270: 3603–3609

    PubMed  CAS  Google Scholar 

  • Robinson HH and Kahn SD (1990) Interplay of substituted conformation and electron affinity in quinone models of quinone reductases. J Am Chem Soc 112: 4728–4731

    CAS  Google Scholar 

  • Savitsky A, Dubinskii AA, Flores M, Lubitz W and Möbius K (2007) Orientation-resolving pulsed electron dipolar high-field EPR spectroscopy on disordered solids: I. Structure of spincorrelated radical pairs in bacterial photosynthetic reaction centers. J Phys Chem B 111: 6245–6262

    PubMed  CAS  Google Scholar 

  • Schenck CC, Parson WW, Holten D, Windsor MW and Sarai A (1981) Temperature dependence of electron transfer between bacteriopheophytin and ubiquinone in protonated and deuterated reaction centers of Rhodopseudomonas sphaeroides. Biophys J 36: 479–489

    PubMed  CAS  Google Scholar 

  • Schmid R and Labahn A (2000) Temperature and free energy dependence of the direct charge recombination rate from the secondary quinone in bacterial reaction centers from Rhodobacter sphaeroides. J Phys Chem B 104: 2928–2936

    CAS  Google Scholar 

  • Schmid R, Goebel F, Warnecke A and Labahn A (1999) Synthesis and redox potentials of methylated vitamin K derivatives. J Chem Soc, Perkin Trans 2 1199–1202

    Google Scholar 

  • Schüler RH, Tripathi GNR, Prebenda MF and Chipman DM (1983) Resonance Raman and molecular orbital studies of the effects of deuteration on the vibrational structure of the p-benzoquinone radical anion. J Phys Chem 87: 5357–5361

    Google Scholar 

  • Sebban P, Maróti P, Schiffer M and Hanson DK (1995) Electrostatic dominoes: Long distance propagation of mutational effects in photosynthetic reaction centers of Rhodobacter capsulatus. Biochemistry 34: 8390–8397

    PubMed  CAS  Google Scholar 

  • Shinkarev VP and Wraight CA (1993) Electron and proton transfer in the acceptor quinone complex of reaction centers of phototrophic bacteria. In: Deisenhofer J and Norris JR (eds) The Photosynthetic Reaction Center, 1, pp 193–255. Academic Press, San Diego

    Google Scholar 

  • Shinkarev VP and Wraight CA (1997) The interaction of quinone and detergent with reaction centers of purple bacteria. I. Slow quinone exchange between reaction center micelles and pure detergent micelles. Biophys J 72: 2304–2319

    PubMed  CAS  Google Scholar 

  • Shopes RJ and Wraight CA (1985) The acceptor quinone complex of Rhodopseudomonas viridis reaction centers. Biochim Biophys Acta 806: 348–356

    PubMed  CAS  Google Scholar 

  • Sinnecker S, Flores M and Lubitz W (2006) Protein-cofactor interactions in bacterial reaction centers from Rhodobacter sphaeroides R-26: Effect of hydrogen bonding on the electronic and geometric structure of the primary quinone. A density functional theory study. Phys Chem Chem Phys 8: 5659–5670

    PubMed  CAS  Google Scholar 

  • Slifkin MA and Walmsley RH (1969) Infra-red studies of quinhydrone type complexes. Spectrochim Acta A 26: 1237–1242

    Google Scholar 

  • Spoyalov AP, Hulsebosch RJ, Shochat S, Gast P and Hoff AJ (1996) Evidence that Ala M260 is hydrogen-bonded to the reduced primary acceptor quinone QA -• in reaction centers of Rb. sphaeroides. Chem Phys Lett 263: 715–720

    CAS  Google Scholar 

  • Stilz HU, Finkele U, Holzapfel W, Lauterwasser C, Zinth W and Oesterhelt D (1994) Influence of M subunit Thr222 and Trp252 on quinone binding and electron transfer in Rhodobacter sphaeroides reaction centres. Eur J Biochem 223: 233–242

    PubMed  CAS  Google Scholar 

  • Stowell MHB, McPhillips TM, Rees DC, Soltis SM, Abresch E and Feher G (1997) Light-induced structural changes in photosynthetic reaction center: Implications for mechanism of electron-proton transfer. Science 276: 812–816

    PubMed  CAS  Google Scholar 

  • Sundberg RJ and Martin RB (1974) Interactions of histidine and other imidazole derivatives with transition metal ions in chemical and biological systems. Chem Rev 74: 471–517

    CAS  Google Scholar 

  • Taly A, Sebban P, Smith JC and Ullmann GM (2003) The position of QB in the photosynthetic reaction center depends on pH: A theoretical analysis of the proton uptake upon QB reduction. Biophys J 84: 2090–2098.

    PubMed  CAS  Google Scholar 

  • Tandori J, Sebban P, Michel H and Baciou L (1999) In Rhodobacter sphaeroides reaction centers, mutation of proline L209 to aromatic residues in the vicinity of a water channel alters the dynamic coupling between electron and proton transfer processes. Biochemistry 38: 13179–13187

    PubMed  CAS  Google Scholar 

  • Tandori J, Maróti P, Alexov E, Sebban P and Baciou L (2002) Key role of proline L209 in connecting the distant quinone pockets in the reaction center of Rhodobacter sphaeroides. Proc Natl Acad Sci USA 99: 6702–6706

    PubMed  CAS  Google Scholar 

  • Thijs R and Zeegers-Huyskens T (1984) Infrared and Raman studies of hydrogen bonded complexes involving acetone, acetophenone and benzophenone. I. Thermodynamic constants and frequency shifts of the vOH and vC=O stretching vibrations. Spectrochim Acta 40A: 307–313

    CAS  Google Scholar 

  • Tiede DM, Vazquez J, Cordova J and Marone PA (1996) Timeresolved electrochromism associated with the formation of quinone anions in the Rhodobacter sphaeroides R26 reaction center. Biochemistry 35: 10763–10775

    PubMed  CAS  Google Scholar 

  • Utschig LM, Thurnauer MC, Tiede DM and Poluektov OG (2005) Low-temperature interquinone electron transfer in photosynthetic reaction centers from Rhodobacter sphaeroides and Blastochloris viridis: Characterization of QB - states by high-frequency electron paramagnetic resonance (EPR) and electron-nuclear double resonance (ENDOR). Biochemistry 44: 14131–14142

    PubMed  CAS  Google Scholar 

  • Van den Brink JS, Hulsebosch RJ, Gast P, Hore PJ and Hoff AJ (1994) QA binding in reaction in reaction centers of the photosynthetic purple bacterium Rhodobacter sphaeroides R26: Investigation with electron spin polarization spectroscopy. Biochemistry 33: 13668–13677

    PubMed  Google Scholar 

  • Van der Est A, Prisner T, Bittl R, Fromme P, Lubitz W, Möbius K and Stehlik D (1997) Time resolved X-, K- and W- band EPR of the radical pair state P700 •+A1 •- of photosystem I in comparison with P865 •+QA •- of bacterial reaction center. J Phys Chem B 101: 1437–1443

    Google Scholar 

  • Van Liemt BS, Boender GJ, Gast P, Hoff AJ, Lugtenburg J and De Groot HJM (1995) 13C Magic angle spinning NMR characterization of the functionally asymmetric QA binding in Rhodobacter sphaeroides R26 photosynthetic reaction centers using site-specific 13C-labeled ubiquinone-10. Biochemistry 34: 10229–10236

    PubMed  Google Scholar 

  • Wakeham MC, Breton J, Nabedryk E and Jones MR (2004) Formation of a semiquinone at the QB site by A- or B-branch electron transfer in the reaction center from Rhodobacter sphaeroides. Biochemistry 43: 4755–4763

    PubMed  CAS  Google Scholar 

  • Waiden SE and Wheeler RA (2002) Protein conformational gate controlling binding site preference and migration for ubiquinone-B in the photosynthetic reaction center of Rhodobacter sphaeroides. J Phys Chem B 106: 3001–3006

    Google Scholar 

  • Warncke K and Dutton PL (1992) Both carbonyl groups are necessary for strong interaction of the semiquinone at the QA site of photosynthetic reaction center protein. Biophys J 57: 571a

    Google Scholar 

  • Warncke K and Dutton PL (1993a) Experimental resolution of the free energies of aqueous solvation contributions to ligand-protein binding: quinone-QA site interactions in the photosynthetic reaction center protein. Proc Natl Acad Sci USA 90: 2920–2924

    PubMed  CAS  Google Scholar 

  • Warncke K and Dutton PL (1993b) Influence of QA site cofactor structure on equilibrium binding, in situ electrochemistry, and electron-transfer performance in the photosynthetic reaction center protein. Biochemistry 32: 4769–4779

    PubMed  CAS  Google Scholar 

  • Warncke K, Gunner MR and Dutton PL (1987) Effect of hydrocarbon tail structure on the affinity of substituted quinones for the QA site in reaction centers of Rhodopseudomonas sphaeroides R-26. In: Biggins J (ed) Progress in Photosynthesis Research, pp 217–220. Martinus Nijhoff, Dordrecht

    Google Scholar 

  • Warncke K, Gunner MR, Braun BS, Gu L, Yu C-A, Bruce JM and Dutton PL (1994) Influence of hydrocarbon tail structure on quinone binding and electron-transfer performance at the QA and QB sites of the photosynthetic reaction center protein. Biochemistry 33: 7830–7841

    PubMed  CAS  Google Scholar 

  • Wells TA, Takahashi E and Wraight CA (2003) Protein control of the redox potential of the primary quinone acceptor in reaction centers from Rhodobacter sphaeroides. Biochemistry 42: 4064–4074

    PubMed  CAS  Google Scholar 

  • Wheeler RA (2001) Quinones and quinoidal radicals in photosynthesis. In: Eriksson LA (ed) Theoretical Biochemistry — Processes and Properties, pp 655–690. Elsevier, Amsterdam

    Google Scholar 

  • Williams JC, Steiner LA and Feher G (1986) Primary structure of the reaction center from Rhodopseudomonas sphaeroides. Proteins 1: 312–325

    PubMed  CAS  Google Scholar 

  • Williams JC, Paddock ML, Feher G and Allen JP (1991) Effects of iron ligand substitutions in reaction centers from Rhodobacter sphaeroides. Biophys J 59: 142a

    Article  Google Scholar 

  • Woodbury NW and Allen JP (1995) The pathway, kinetics and thermodynamics of electron transfer in wild type and mutant reaction centers of purple nonsulfur bacteria. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 527–557. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Woodbury NW, Becker M, Middendorf D and Parson WW (1985) Picosecond kinetics of the initial photochemical electrontransfer reaction in bacterial photosynthetic reaction centers. Biochemistry 24: 7516–7521

    PubMed  CAS  Google Scholar 

  • Woodbury NW, Parson WW, Gunner MR, Prince RC and Dutton PL (1986) Radical-pair energetics and decay mechanisms in reaction center containing anthraquinones or benzoquinones in place of ubiquinone. Biochim Biophys Acta 851: 6–22

    PubMed  CAS  Google Scholar 

  • Wraight CA (1978) Iron-quinone interactions in the electron acceptor region of bacterial photosynthetic reaction centers. FEBS Lett 93: 283–288

    CAS  Google Scholar 

  • Wraight CA (1979) Electron acceptors of bacterial photosynthetic reaction centers II. H+ binding coupled to secondary electron transfer in the quinone acceptor complex. Biochim Biophys Acta 548: 309–327

    PubMed  CAS  Google Scholar 

  • Wraight CA (1982) The involvement of stable semiquinones in the two-electron gates of plant and bacterial photosystems. In: Trumpower BL (ed) Function of Quinones in Energy Conserving Systems, pp 181–197. Academic Press, New York

    Google Scholar 

  • Wraight CA (2004) Proton and electron transfer in the acceptor quinone complex of bacterial photosynthetic reaction centers. Frontiers Biosci 9: 309–327

    CAS  Google Scholar 

  • Wraight CA (2005) Intraprotein proton transfer — Concepts and realities from the bacterial photosynthetic reaction center. In: Wikström M (ed) Biophysical and Structural Aspects of Bioenergetics, pp 273–313. Royal Society of Chemistry, Cambridge, U.K.

    Google Scholar 

  • Xu Q and Gunner MR (2000) Temperature dependence of the free energy, enthalpy, and entropy of P+QA - charge recombination in Rhodobacter sphaeroides R-26 reaction centers. J Phys Chem B 104: 8035–8043

    CAS  Google Scholar 

  • Xu Q and Gunner MR (2001) Trapping conformational intermediate states in the reaction center protein from photosynthetic bacteria. Biochemistry 40: 3232–3241

    PubMed  CAS  Google Scholar 

  • Xu Q and Gunner MR (2002) Exploring the energy profile of the QA - to QB electron transfer reaction in bacterial photosynthetic reaction centers: pH dependence of the conformational gating step. Biochemistry 41: 2694–2701

    PubMed  CAS  Google Scholar 

  • Xu Q, Baciou L, Sebban P and Gunner MR (2002) Exporing the energy landscape for QA - to QB electron transfer in bacterial photosynthetic reaction centers: Effect of substrate position and tail length on the conformational gating step. Biochemistry 41: 10021–10025

    PubMed  CAS  Google Scholar 

  • Zachariae U and Lancaster CRD (2001) Proton uptake associated with the reduction of the primary quinone QA influences the binding site of the secondary quinone QB in Rhodopseudomonas viridis photosynthetic reaction centres. Biochim Biophys Acta 1505: 280–290

    PubMed  CAS  Google Scholar 

  • Zadorozhnyi BA and Ishchenko IK (1965) Hydrogen bond energies and shifts of the stretching vibration bands of C=O groups. Optics & spectroscopy (Eng Translation) 19: 306–308

    Google Scholar 

  • Zhao X and Kitagawa T (1998) Solvent effects of 1,4-benzoquinone and its anion radicals probed by resonance Raman and absorption spectra and their correlation with redox potentials. J Raman Spectrosc 29: 773–780

    CAS  Google Scholar 

  • Zhao X, Imahori H, Zhan C-G, Sakata Y, Iwata S and Kitagawa T (1997a) Resonance Raman and FTIR spectra of isotope-labeled reduced 1,4-benzoquinone and its protonated forms in solution. J Phys Chem A 101: 622–631

    CAS  Google Scholar 

  • Zhao X, Ogura T, Okamura M and Kitagawa T (1997b) Observation of the resonance Raman spectra of the semiquinones QA •- and QB •- in photosynthetic reaction centers from Rhodobacter sphaeroides R26. J Am Chem Soc 119: 5263–5264

    CAS  Google Scholar 

  • Zhu Z and Gunner MR (2005) The energetics of quinone dependent electron and proton transfers in Rhodobacter sphaeroides photosynthetic reaction centers. Biochemistry 44: 82–96

    PubMed  CAS  Google Scholar 

  • Zhu Z-Y and Karlin S (1996) Clusters of charged residues in protein three-dimensional structures. Proc Natl Acad Sci USA 93: 8350–8355

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Colin A. Wraight .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer Science + Business Media B.V

About this chapter

Cite this chapter

Wraight, C.A., Gunner, M.R. (2009). The Acceptor Quinones of Purple Photosynthetic Bacteria — Structure and Spectroscopy. In: Hunter, C.N., Daldal, F., Thurnauer, M.C., Beatty, J.T. (eds) The Purple Phototrophic Bacteria. Advances in Photosynthesis and Respiration, vol 28. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-8815-5_20

Download citation

Publish with us

Policies and ethics